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Miranda Haggerty was diving through a kelp forest, and noticed that many kelp bore a large number of tiny limpets that were housed in small scars that they (or a fellow-limpet) had excavated on the kelp’s surface. This got her thinking about how these scars might affect the kelp, and equally relevant, whether there were any limpet predators that might lend the kelp a hand (or a mouth) by removing limpets.

A limpet grazes on a kelp frond. Credit: Jerry Kirkhart

Feather boa kelp (Egregia menziesii) is a foundation species within the subtidal marine system off the California coast, providing food and habitat for many species that live on or among its fronds. The tiny seaweed limpet, Lottia insessa, specializes on feather boa kelp, grazing on its fronds and living within the scars. Many invertebrates and fish live within the kelp forest, but the most abundant fish is the señorita, Oxyjulis californica. Haggerty wondered whether the señorita might benefit the kelp (directly) by removing limpets, or (indirectly) by scaring limpets away – what ecologists call a trait-mediated indirect interaction.

The first order of business was to determine whether the limpets were actually harming the kelp. Haggerty and her colleagues approached this in two ways. First they chose 94 kelp plants from kelp forests off the California coast. From each individual they chose one grazed and one ungrazed frond (each 3 m long). Grazed fronds averaged 5-10 scars and at least 2 limpets per meter of length. Every three weeks they visited their kelp to score for broken fronds. In 29 of 30 cases, the grazed frond broke before the ungrazed frond (in the remaining cases the entire plant was missing, or both fronds broke and the researchers could not tell which had broken first).

But the researchers were concerned that perhaps limpets chose to graze on weaker fronds, so the breakage was not caused by grazing scars, but by limpet choice. To account for this concern, Haggerty and her colleagues chose 43 ungrazed kelp plants, placed three limpets on one frond, and chose a second, equal-sized frond as an unmanipulated control. Once again, they visited their plants every three weeks, and discovered that grazed fronds broke first in all 20 pairs that the sequence of frond breakage could be determined. Clearly, limpet grazing is bad news for feather boa kelp.

How does the señorita fit into this system? The researchers designed a laboratory experiment to address this question. They used 10 large tanks (1700 L), and set up five different experimental treatments to compare direct effects of predation, and indirect effects of predator presence, on limpet grazing, and ultimately on kelp survival. To isolate the direct effects of predation from the indirect effects of predator cues on limpets, Haggerty and her colleagues placed four kelp fronds into fish exclosure cages, which were housed in the large tanks, and placed three limpets onto some of these fronds. To mimic actual predation (CE treatment in Table below), they removed limpets by hand at a constant rate typical of señorita predation. For the NCE treatment (testing indirect effects of predator presence) they introduced señorita into the large tank so the limpets experienced the predator cues, but were not eaten. The different treatments are summarized in the table below. These experiments ran for one week and each treatment was replicated 10 times.

Each day the researchers monitored the number of limpets and grazing scars. After one week, Haggerty and her colleagues counted the number of grazing scars, and measured the breaking strength of each frond by clamping the frond’s end to a table and pulling on the opposite end with a spring scale until it broke. They then recorded the amount of force needed to break the frond.

Not surprisingly, the predator control (PC) kelp (limpets present without señorita) had the most scars and lost the greatest amount of tissue. Kelp receiving the consumptive predator effect treatment (CE) had fewer scars and lost less tissue than PC. But interestingly, kelp receiving NCE and TPE treatments had significantly fewer scars than the CE kelp, and were statistically indistinguishable from each other. Thus, in the laboratory, the presence of señorita cues (NCE treatment) was more important than actual predation (CE treatment) in reducing kelp scarring and tissue consumption (top and middle graph below). As a result, the NCE treated kelp were stronger (had greater breaking strength) than were the CE treated kelp (bottom graph below).

Haggerty and her colleagues replicated this experiment, with a few experimental design modifications, in a field setting. As with the laboratory experiment we’ve just discussed, the researchers found a very strong non-consumptive effect. The researchers suspect that these limpets respond to chemical cues emitted by their señorita predators. They could not respond to many types of sensory cues because they lack auditory organs, and the experimental design prevented fish from transmitting any shadows (visual cues) or vibrational cues. In addition previous studies have shown that some limpet species use chemoreception for predator avoidance, foraging and homing. However, the nature of this chemical cue is yet to be discovered for this predator-prey system.

Schooling señorita. Credit: Miranda Haggerty

Trophic cascades occur when the effects of one species on another species cascade down through the ecosystem. In this case, señorita predators directly and indirectly reduce limpet density, which increases the survival of kelp – a foundation species for this ecosystem. The researchers point out that this trophic cascade only occurs in the southern feather boa kelp range, because señorita are absent further north. We don’t know if limpets have other predators in the northern range, but we do know that the kelp are structurally more robust further north, so they (and the ecosystem) may be relatively immune to limpet-induced destruction.

If you’re ever feeling sorry for yourself, you should know that things could have been much worse; you could have been the brown seaweed, Silvetia compressa. So many problems! Ocean waves come crashing over you, threatening to pull you off your life-sustaining substrate. Ocean tides recede, exposing you to harsh sun and dangerously dry conditions. Perhaps worst of all, the fearsome predator Tegula funebralis eats away at your body, and you are powerless to defend yourself from its savage ravages.

As it turns out, Silvetia is not so powerless after all. After being partially grazed by Tegula, the seaweed can induce defenses that reduce its palatability. From prior work, Emily Jones noticed that seaweed from northern California shorelines was much more sensitive to grazing than was seaweed from southern California shorelines. It took fewer grazing snails to elicit palatability reduction in northern Silvetia than it did in southern Silvetia. She decided to focus her PhD work with Jeremy Long on documenting these geographic differences, and figuring out why they exist.

Environmental conditions vary along the California coast. Northern seaweed populations experience cooler temperatures (air ~5-20 °C; water ~10-12 °C) and more nutrients (nitrate levels up to 40 umol/L) than do southern populations (air 5-37 °C; water ~14-20 °C; nitrate levels < 2 umol/L). In addition, Jones and Long surveyed Tegula abundance at three northern California and three southern California sites, counting every snail in 20 quadrats placed in the low, mid and high intertidal zone at each of the six sites (360 0.25 X 0.25m quadrats in total) . They discovered that seaweed was much more likely to encounter Tegula along northern coastlines.

Given these differences in snail abundance, we can now understand why Silvetia is more sensitive in its northern range to Tegula grazing. But how strong are these differences in sensitivity? Jones and Long developed a simple paired-choice feeding preference assay to test for differences in palatability. At each location (north and south), the researchers gave test snails a choice between feeding on seaweed that had been previously grazed by either 1, 4, 7, 10 or 13 Tegula snails, or to feed on seaweed with no grazing history. The test snails grazed for five days, and the researchers measured the amount of seaweed consumed for each group. They discovered that even a little bit of previous grazing (the 1-snail treatment) made northern test snails prefer non-grazed northern Silvetia, while only high levels of previous grazing (the 10 and 13-snail treatments) had similar effects on southern snails tested on southern Silvetia.

These findings raised the question of whether the cooler and more nutrient-rich environmental conditions at the northern site were somehow causing this difference in consumption of previously-grazed seaweed. The researchers designed a series of common garden experiments at the Bodega Marine Laboratory, in which seaweed from both locations were tested in the same environment. Silvetia was exposed to grazing by two snails, or by no snails for 14 days. When test snails were given the choice of non-grazed or previously-grazed northern Silvetia, they much preferred eating non-grazed Silvetia. In contrast, they showed no preference when given a similar choice between non-grazed or previously-grazed southern Silvetia. This indicates that seaweed from the north are responding more to grazing by reducing palatability than are seaweed from the southern locations.

Amount of previously-grazed and non-grazed northern and southern Silvetia eaten by Tegula in paired choice tests.

In theory, there could be a tradeoff between induced defenses, such as reduction in palatability in response to grazing, and constitutive defenses, which an organism expresses all of the time. Examples of constitutive defenses are thorns or spines in plants, and cryptic coloration or body shape in many insects. Jones and Long found no evidence for such a tradeoff; in contrast southern Silvetia actually had lower levels of constitutive defenses, as both northern and southern Tegula strongly preferred eating southern Silvetia in paired choice tests.

Amount of northern and southern Silvetia eaten by northern and southern Tegula in paired choice tests.

These geographic differences in seaweed sensitivity to grazing are probably due to long-term differences in environmental history. Southern Silvetia seaweeds live in stressful conditions (high temperatures and low nutrients), and the physiological cost of mounting an induced defense against low and moderate levels of grazing may be too high to be worthwhile. We also don’t know what the overall grazing rates are in the north versus the south, and importantly, how variable the grazing rates are in each location. Highly variable grazing rates would select for a strong set of induced responses, which could be turned on and off as needed, allowing seaweed, or any plant, to defend itself against new or more hungry herbivores moving into their environment.

Many plants shed their young embryos (seeds) into the soil where they may accumulate in a dormant (non-growth) state over years before germinating (resuming growth and development). Ecologists describe this collection of seeds as a seed bank. Marina LaForgia describes how scientists were able to germinate and grow to maturity some 32,000 year old Silene stenophylla seeds that was stashed, probably by an ancient squirrel, in the permafrost! With increased climatic variation predicted by most climate models, she wanted to know how environmental variability might affect germination of particular groups of species within a community. In addition, she and her colleagues recognized that most ecological studies investigate community responses to disturbances by looking at the aboveground species. It stands to reason that we should consider the below-surface seed bank as a window to how a community might respond in the future.

Some seedlings coming up from the seed bank. Credit:Marina LaForgia.

Seed banks can be viewed as a bet-hedging strategy that spreads out germination over several (or many) years to reduce the probability of catastrophic population decline in response to one severe disturbance, such as drought, flood or fire. In some California annual grassland communities, species diversity is dominated by annual forbs – nonwoody flowering plants that are not grasses. Many forbs produce seeds that can lie dormant in the seed banks for several years. Though these forbs are the most diverse group, there are also about 15 species of exotic annual grasses that dominate the landscape in abundance and cover. These grasses dominate because they produce up to 60,000 seeds per m2, they grow very quickly, and they build up a layer of thatch that suppresses native forbs. However, seeds from these grasses cannot lie dormant in the seed bank for very long.

Area of field site dominated by Delphinium (purple flower) and Lasthenia (yellow flower). Looking closely you can also see some tall grasses rising. Credit Marina LaForgia.

How is drought affecting these two major components of the plant community? LaForgia and her colleagues answered this question by collecting seeds from a northern California grassland at the University of California McLaughlin Natural Reserve in fall 2012 (beginning of the drought) and fall 2014 (near the end of the drought). They used a 5-cm diameter 10-cm deep cylindrical sampler to collect soil and associated seeds from 80 different plots. The researchers also used these same plots to estimate aboveground-cover, and to identify the aboveground species that were present. The research team germinated and identified more than 11,000 seeds.

Plants germinating in the greenhouse. Credit Marina LaForgia.

The researchers knew from previous work on aboveground vegetation that exotic annual grasses declined very sharply in response to drought. In contrast, the native forbs did relatively well, in part depending on their specific leaf area (SLA) – a measure of relative leaf size, with low SLA plants conserving water more efficiently. It seemed reasonable that these same patterns would be reflected belowground. Recall that most grass seeds are incapable of extended dormancy, while many forbs can remain dormant for several years. Consequently, LaForgia and her colleagues expected that grass abundance in the seed bank would decline more sharply than would forb abundance. In addition, they expected that high SLA forbs would not do as well as low SLA forbs during drought.

The researchers discovered very sharp differences between the two groups over the course of the drought. Exotic annual grasses declined sharply in the seed bank, while native annual forb abundance tripled. Aboveground cover of grasses declined considerably, while aboveground cover of forbs increased modestly. Clearly the exotic grasses were suffering from the drought, while the forbs were doing quite well.

(a) Seed bank abundance of grasses (red circles) and forbs (blue triangles) at beginning of drought (2012) and near end of drought (2014). (b) Percent cover of grasses (red circles) and forbs (blue triangles) at beginning of drought (2012) and near end of drought (2014). Data are based on samples from 80 plots. Error bars indicate one standard error.

We can see these differences on an individual species basis, with most of the grasses declining modestly or sharply in abundance, while most of the forbs increased.

Mean change in seed bank abundance per species based on 15 exotic grass species and 81 native forb species.

It is not surprising that the grasses do so poorly during the drought. Presumably, less water causes poorer germination, growth, survival and seed production. In addition, because grass seeds have a low capacity for dormancy, grass abundance will tend to decrease in the seed bank very quickly with such a low infusion of new seeds.

But why are the forbs actually doing better with less water available to them? One explanation is that grass abundance and cover declined sharply, causing the forbs to experience reduced competition with grasses that might otherwise inhibit their growth, development and reproductive success. The tripling of native forbs in the seed bank was much greater than the 14% increase in aboveground forb cover. The researchers reason that the drought caused many of the forb seeds to remain dormant, leading to them building up in the seed bank. This was particularly the case for low SLA forbs, which increased much more than did high SLA forbs in the seed bank.

We can understand exotic grass behavior in the context of their place of origin – the Mediterranean basin, which tends to have wet winters. In that environment, natural selection favored individuals that germinated quickly, grew fast and made lots of babies. Since their introduction to California in the mid 1800s, 2014 was the driest year on record. It will be fascinating to see if these exotic grasses can recover when, and if, wetter conditions return. Can we bank on it?

Given recent discussions between Donald Trump and Kim Jong-un about whose button is bigger, many of us with entomological leanings have revisited the question of what insects are most likely to dominate a post-nuclear world. Cicadas have a developmental life history that predisposes them to survival in the long term because some species in the eastern United States spend many subterranean years as juveniles (nymphs), feeding on the xylem sap within plants’ root systems. Magicicada nymphs live underground for 13 or 17 years, depending on the species, before digging out en masse, undergoing one final molt, and then going about the adult business of reproduction. This life history of spending many years underground followed by a mass emergence has not evolved to avoid nuclear holocausts while underground, but rather to synchronize emergence of billions of animals. Mass emergence causes predator satiation, an anti-predator adaptation in which predators are gastronomically overwhelmed by the number of prey items, so even if they eat only cicadas and nothing else, they still are able to consume only a small fraction of the cicada population.

Less well-known are the protoperiodical cicadas (subfamily Tettigadinae) of the western United States that are abundant in some years, and may be entirely absent in others. Jeffrey Cole has studied cicada courtship songs for many years, and during his 2003 field season noted that localities that had previously been devoid of cicadas now (in 2003) hosted huge numbers of six or seven different species. He returned to those sites every year and high diversity and abundance reappeared in 2008 and 2014. This flexible periodicity contrasted with their eastern Magicicada cousins, and he wanted to know what stimulated mass emergence.

Cole and his graduate student, Will Chatfield-Taylor, considered two hypotheses that might explain protoperiodicity in southern California (where they focused their efforts). The first hypothesis is that cicada emergence is triggered by heavy rains generated by El Niño Southern Oscillation (ENSO), a large-scale atmospheric system characterized by high sea temperature and low barometric pressure over the eastern Pacific Ocean. ENSO has a variable periodicity of 4.9 years, which roughly corresponds to the timing Cole observed while doing fieldwork. The second hypothesis recognized that nymphs must accumulate a set amount of xylem sap from their host plants to complete development. Sap availability depends on precipitation, and this accumulation takes several years in arid habitats. So while ENSO may hasten the process, the key to emergence is a threshold amount of precipitation over a several year timespan.

Working together, the researchers were able to identify seven protoperiodical species by downloading museum specimen data (including where and when each individual was collected) from two databases (iDigBio and SCAN). They also used data from several large museum collections, which gave them evidence of protoperiodical cicada emergences back to 1909. Based on these data, Chatfield-Taylor and Cole constructed a map of where these protoperiodical cicadas emerge.

Maps of five emergence localities discussed in this study.

The researchers tested the hypothesis that protoperiodical cicada emergences follow heavy rains triggered by ENSO by going through their dataset to see if there was a correlation between ENSO years and mass cicada emergences. Of 20 mass cicada emergences since 1918, only five coincided with ENSO events, which is approximately what would be expected with a random association between mass emergences and ENSO. Scratch hypothesis 1.

Let’s look at the second hypothesis. The researchers needed reliable precipitation data between years for which they had good evidence that there were mass emergences of their seven species. Using a statistical model, they discovered that 1181 mm was a threshold for mass emergences, and that three years was the minimum emergence interval regardless of precipitation. Only after 1181 mm of rain fell since the last mass emergence, summed over at least three years, would a new mass emergence be triggered.

The nice feature of this model is that it makes predictions about the future. For example, the last emergence occurred in the Devil’s punchbowl vicinity in 2014. Since then that area has averaged 182.2 mm of precipitation per year. If those drought conditions continue, the next mass emergence will occur in 2021 at that locality, which is longer than its historical average. Only time will tell. Hopefully Mr. Trump and Mr. Jong-un will be able to keep their fingers off of their respective buttons until then.